Fear conditioning, persistence of disruptive behavior and psychopathic traits: an fMRI study

Abstract

Children diagnosed with Disruptive Behavior Disorders (DBD), especially those with psychopathic traits, are at risk of developing persistent and severe antisocial behavior. Deficient fear conditioning may be a key mechanism underlying persistence, and has been associated with altered regional brain function in adult antisocial populations. In this study, we investigated the associations between the neural correlates of fear conditioning, persistence of childhood-onset DBD during adolescence and psychopathic traits. From a cohort of children arrested before the age of 12 years, participants who were diagnosed with Oppositional Defiant Disorder or Conduct Disorder in previous waves (mean age of onset 6.5 years, s.d. 3.2) were reassessed at mean age 17.6 years (s.d. 1.4) and categorized as persistent (n=25) or desistent (n=25) DBD. Using the Youth Psychopathic Traits Inventory and functional magnetic resonance imaging during a fear conditioning task, these subgroups were compared with 26 matched healthy controls from the same cohort. Both persistent and desistent DBD subgroups were found to show higher activation in fear processing-related brain areas during fear conditioning compared with healthy controls. In addition, regression analyses revealed that impulsive-irresponsible and grandiose-manipulative psychopathic traits were associated with higher activation, whereas callous-unemotional psychopathic traits were related to lower activation in fear-related areas. Finally, the association between neural activation and DBD subgroup membership was mediated by impulsive-irresponsible psychopathic traits. These results provide evidence for heterogeneity in the neurobiological mechanisms underlying psychopathic traits and antisocial behavior and, as such, underscore the need to develop personalized interventions.

Fear extinction, persistent disruptive behavior and psychopathic traits: fMRI in late adolescence

“…However, emotional hyporeactivity characterizes only one part of persistent offenders (Hodgins, 2007). Hyperreactivity during fear acquisition has been found in antisocial juveniles from lower social class (Raine and Venables, 1981) and in our previous fear acquisition study (Cohn et al, 2013). In summary, there is some evidence for aberrant fear responsiveness in subgroups of antisocial individuals, but the current literature on fear extinction in antisocial individuals is limited by an exclusive focus on the emotionally hyporeactive subgroup.…”

“…that its dimensions are distinctly associated with behavioral criterion variables (Patrick et al, 2005;Hicks and Patrick, 2006) and regional brain function (Carré et al, 2013;Cohn et al, 2013). Indeed, we found that neural responses during fear acquisition were positively associated with GM and II psychopathic traits and negatively with CU psychopathic traits (Cohn et al, 2013). However, nothing is known about the associations between the different psychopathic traits and brain activation during fear extinction.…”

“…As such, it seems relevant to investigate whether persistence of DBD in our hyperreactive sample is associated with an inability to down-regulate previously acquired fear responses in the face of changing contingencies. Importantly, our previous study (Cohn et al, 2013) also showed that group differences in neural responses during fear acquisition were largely explained by differences in psychopathic traits. In addition, various studies have shown that psychopathic traits are not a unitary construct: i.e.…”

“…We have recently shown (Cohn et al, 2013) that neural activation during fear conditioning does not differentiate adolescents with a persistent or a desistent Disruptive Behavior Disorder [DBD; Oppositional Defiant Disorder (ODD) or CD] compared with HCs: both DBD-persisters (DBD-p) and DBD-desisters (DBD-d) showed increased activation of the fear circuit in response to cues predicting an aversive electric unconditioned stimulus vs neutral cues. Importantly, we also found that these neural activation patterns were related to the presence of II psychopathic traits, and group differences in neural activation were in fact mediated by these II traits.…”

“…In this report, we present extinction data from our fear conditioning experiment (Cohn et al, 2013), that is, fMRI data from a large cohort of childhood arrestees followed up in late adolescence, allowing the distinction between DBD-p, DBD-d and HCs. Because extinction studies in antisocial samples are scarce, we used a basic paradigm assessing extinction learning-relying on function of the basic fear neurocircuitry [amygdala, insula and anterior cingulate cortex (ACC)]-rather than its consolidation or modulation-relying on the ventromedial prefrontal cortex and hippocampus, respectively (Quirk and Mueller, 2008;Delamater and Westbrook, 2014).…”